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Evolutionary Development of the Mammalian Presternum Zeynep Metin Yozgyur Submitted in Partial Fulfillment of the Prerequisite for Honors in Biological Sciences under the advisement of Emily Buchholtz April 2019 This material is copyrighted by Zeynep Yozgyur and Emily Buchholtz, April 25, 2019. © 2019 Zeynep Yozgyur 1 Abstract The mammalian sternum has undergone a reduction in relative size and complexity over evolutionary time. This transformation was highly variable across species, generating multiple, controversial interpretations. Some authors claim that the evolutionary reduction led to loss of presternal elements, while others believe that all, or some, presternal elements were fused into a structure ambiguously referred to as the “manubrium”, a term adopted from the post- interclavicular unit of pre-mammalian ancestors. Previous work on the Paramylodon harlani presternum revealed a composite presternum and identified three elements - mediocranial, mediocaudal and lateral - each with a different developmental origin and marginal articulation. This project used medical and micro CT scans to determine if these elements are conserved across species and if there is a characteristic histology associated with each. All three elements were identified in humans based on their locations and articulations. Their fusion during ontogeny was documented. Elements could not be associated with a characteristic histology. Instead, histology appears to reflect the mechanical forces to which different regions of the presternum are subjected, whatever their developmental origin. This opens the possibility that the presternum can be used to infer the limb use and locomotor style of extinct taxa. These lines of evidence indicate that the reduction of relative sternal size seen over evolutionary time has not led to element loss. Instead, three conserved elements with unique developmental origins and articulations are present in a composite presternum. Further, this reasoning suggests that the use of the term “manubrium” should be abandoned as ambiguous and instead when referring to specific areas on the presternum the terms interclavicle, sternal bands, and lateral elements should be used. 2 Contents 1. Introduction 4 1.1. Sternal anatomy in major mammalian groups …………………………………………….………….4 1.2. Overview of the developmental biology of the mammalian sternum ……………………. 8 1.3. Detailed development of major sternal units ………………………………………………..….……9 1.4. Bone remodeling ………………………………………………………………………….…………..………... 10 1.5. Theories of presternal evolution …………………………………………………………………………..11 1.6. Homology ……………………………………………………………………………………………..……………..15 1.7. Variations of the human presternum ………………………………………………..………………… 15 2. Materials and Methods 16 2.1. Human medical CT scans ……………………………………………………………………….…….……… 16 2.2. Comparative micro CT scans …………………………………………………………….…………………. 18 3. Results 21 3.1. Presternal patterns. …………………………………………………………………………………..………...21 3.2. Ontogenetic changes with presternal patterns ……………………………………..……………. 25 3.3. Comparative Sternal Series …………………………………………………………………..……………..29 4. Discussion 46 4.1. Multiple eutherian taxa possess composite presterna ……………………………………..…. 46 4.2. Progressive fusion of elements is characteristic …………………………………………..……… 46 4.3. Conserved number and positional relationships of presternal elements ………..…… 47 4.4. Element identification can be proposed from location and articular contacts …..… 47 4.5. Variable ontogenetic sequence and timing of element fusion …..………………………… 48 4.6. Trabecular histology does not support variation in presternal elements based on developmental origin …………………………………………………………………………………………….….. 48 4.7. The term “manubrium” is not appropriate for referencing the presternum ……..… 50 5. Conclusions 51 6. Literature Cited 52 7. Acknowledgements 55 3 1. Introduction The mammalian sternum is a highly variable and poorly understood anatomical unit in the thoracic ventral midline. Its differential classification as either axial or appendicular, and the disparate theories of its evolutionary transformation, are signals of its controversial interpretation. What is clear is that over mammalian evolutionary history the sternum as a whole has been reduced in relative size, and that the presternal subunit of the sternum has been reduced in element count. This project examines the hypothesis that the evolutionary reduction in presternal element count is primarily the result of the fusion of three ancestral elements, each with a discrete developmental origin and an articulation to a dedicated lateral structure. If supported, it suggests that evolutionary retention of presternal elements may reflect their unique developmental interactions. The project also tests the hypothesis that presternal elements are histologically differentiated, allowing reconstruction of an element’s extent even after ontogenetic fusion. The project integrates classical and tomographic anatomical descriptions with the theory of mesodermal pattern domains recently embraced by developmental biologists. Because authors have assigned many different names to sternal, and especially presternal, structures, the default terminology below is adopted for this project, as demonstrated on the human skeleton (Fig. 1). Figure 1. Sternal anatomy. A, generalized musculoskeletal anatomy of the human sternum, modified from https://tinycards.duolingo.com. B, Presternal structure and lateral articulating elements of Weaver Collection specimen W136, a 24.29-year-old male. 1.1. Sternal anatomy in major mammalian groups. Most taxonomic identifications of fossils occur on the basis of cranial and dental elements, and less often on postcranial elements (Gaetano et al., 2018). Based on the structure of the skull, three major groups of amniotes found in the Paleozoic Era have been identified: synapsid, anapsid, and diapsid. These groups are differentiated on the basis of temporal openings of the skull. The synapsid group, which has a single temporal opening, includes the early non-mammalian basal synapsids -- dicynodonts and cynodonts, as well as the living crown mammals – monotremes, marsupials, and eutherians (Fig. 2) (Angielczyk, 2009). 4 Figure 2. Simplified phylogeny of synapsid reptiles and their mammalian descendants. Modified from Angielczyk 2009 (Fig. 4B, p. 261). The fossil record of mammals shows evidence of major reorganizations in the musculoskeletal system of the ventral shoulder girdle (Sereno, 2006). Fossil records of synapsid sterna are rare, but those that exist show an evolutionary sequence of an ancestral sternum that was restricted to the interclavicle in basal synapsids with a sprawling gait, an ‘intermediate’ sternum with an interclavicle that contacts a unit referred to as the “manubrium” and sternal bands in fossil cynodonts and living monotremes, and a sternum with reduced size and number of elements in placentals, suggesting adoption of parasagittal locomotion (Sereno, 2006). Sternal elements are known for the early sphenacodontid synapsid Dimetrodon (Romer, 1956; Angielczyk, 2009) and for the cynodont Diademodon (Gaetano et al., 2018). The Dimetrodon sternum (Fig. 3) consists of a single, presternal element, the interclavicle. Its wide anterior end is slightly concave, and its posterior end is long, narrow and flat. It was identified as an interclavicle due to its surfaces for articulation with the large clavicles on its anterior end. Laterally it articulates with the scapula and coracoid elements of the dorsal shoulder girdle. The other presternal elements present in living mammals - the “manubrium” and the sternal bands - are not present, and there is no connection between the presternum and the rib cage. The sternal elements of the cynodont Diademodon, known from a nearly complete specimen, were described by Gaetano et al. (2018). The left clavicle is convex and still attached to the interclavicle (Fig. 4). The interclavicle is preserved in its full form. In contrast to Dimetrodon, another presternal element is present: a “manubrium” separated into left and right halves. The left half is medially displaced; on its lateral side there is a projection of bone which is interpreted by Gaetano et al. (2018) as the proximal end of the first sternal cartilage. There is no visible suture between the thoracic rib and the “manubrium.” The second rib is fused with 5 Figure 3. Sternal anatomy in Dimetrodon. A, dorsal and ventral views of the interclavicle of D. gagashomogenus from Hunt and Lucas (2005). B, schematic of the interclavicle and the articulating clavicle (Cl) and coracoid (Co), modified from Romer (1956). C, skeletal reconstruction of Dimetrodon from Romer (1927). and positioned posteriorly to the preseternum. The right half of the “manubrium” is not in its natural position, but rather rotated to the right. The fact that there are two presternal elements that are separated indicates that these halves were originally bilaterally paired. As will be described below, this trait is characteristic of sternal bands, which originate as two unsegmented paired elements. Figure 4. Sternal anatomy of Diademodon in dorsal view, modified from Gaetano et al. (2018). A, diagram of bone elements. B, fossil in dorsal view. cl = clavicle; icl = interclavicle; m(l) = left “manubrium”, m(r) = right “manubrium”; r1, r2 = thoracic ribs 1, 2, etc.; r1f = rib 1 facet. Scale bar = 10mm. The sterna of living monotremes closely resemble that of the cynodont Diademodon in that they possess a large interclavicle, a discrete “manubrium,” and a string

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